Development of D. rapae on aphids feeding on different host plants

We could not measure performance of D. rapae on So. lycopersicum as aphid survival was too low. Most life-history traits did not differ significantly among D. rapae that parasitized or emerged from aphids feeding on B. napus, B. oleracea, B. nigra, or S. arvensis. Parasitism rate estimated as % parasitized aphids after 5 days (mean ± SE = 45 ± 3 %) or at mummy stage (49 ± 3 %; Fig. 2a), survival rate from egg to adult (86 ± 2 %), sex ratio expressed as % females (46 ± 4 %), and longevity (7.28 ± 0.19 days) of the resulting adults did not differ between plant species (N = 108 plants and P > α0.05/6 = 0.008 for all comparisons between Brassicaceae). Unexpectedly, development time from egg to mummy was shorter on B. napus and S. arvensis for the male parasitoids (ANOVA, df = 3, F = 8.83, P < 0.001), while differences were not significant for the females (F = 3.14, P = 0.37; Fig. 2b). Development time from mummy to adult was also shorter on B. napus and B. nigra for both males (F = 9.11, P < 0.001) and female parasitoids (F = 8.96, < 0.001; Fig. 2c). The resulting female parasitoids were larger when the aphids fed on B. napus (F = 8.87, P = 0.03), while male parasitoids were larger on S. arvensis (F = 9.76, P = 0.02; Fig. 2d).

2.5. Discussion

In contrast with our initial hypothesis, M. persicae did not perform better on the two cultivated Brassicaceae species, B. napus and B. oleracea. Differences in life-history traits translated into differences in population growth rates with rm significantly smaller on B. napus compared to the three other Brassicaceae (Fig. 1d). Moreover, even though M. persicae is considered as a generalist aphid feeding on a large number of host plants, its development seemed hampered on So. lycopersicum (Fig. 1). Similarly, performance of the parasitoid D.

rapae was affected by the plant on which its host was feeding. Parasitism rate tended to be higher on B. napus and B. oleracea (Fig. 2a). Male development time from egg to mummy and from mummy to adult was shorter on B. napus (Fig. 2b and 2c), and female parasitoids were larger on B. napus (Fig. 2d). Thus, in opposite with the results observed for the aphid, B.

napus seemed a good host plant species for D. rapae even though the impact of the plant on the parasitoid fitness was not as clear as for the herbivore. Previous studies have also shown

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that parasitoids are less affected than the herbivores by host plant characteristics (Barbosa et al., 1986; Harvey, 2005; Gols & Harvey, 2009, Schädler et al., 2010).

Our results contrast with previous studies that have shown that M. persicae develops better on cultivated species, including B. napus and B. oleracea, compared to the wild species such as B. nigra, B. fruticulosa, and B. spinescens (Cole, 1997). Cole’s results indicate a significant negative correlation between the intrinsic growth rate of M. persicae and the concentrations of some glucosinolates in Brassica species or cultivars. Other authors have observed also a negative impact of plant secondary compounds, in particular GLS or their breakdown products, on population growth rate of M. persicae. Insect performance was negatively related to GLS concentrations in B. oleracea (van Emden, 1972 cited in Feeny, 1977), Arabidopsis thaliana (Mewis et al., 2005; Kim et al., 2008), and B. oleracea, B. napus, B. nigra and S. alba (Hodge et al., 2006). In our study, aphid performance did not seem related to the glucosinolate concentrations, as M. persicae population growth rate was significantly lower on B. napus, the species characterized by the lowest GLS concentrations (Le Guigo et al., 2011). However, differences in GLS profiles might also be important (Kuśnierczyk et al., 2007; Poelman et al., 2009). In our study, B. napus and B. nigra are rich in aliphatic GLS, and S. arvensis contains mostly one aromatic GLS (G. Guéritaine and J. Le Corff, unpublished data). Thus, we could have expected the lowest aphid population growth rate on B. oleracea because this cultivar is characterized by the presence of indole GLS, known to be particularly toxic to phloem-feeding insects (Kim et al., 2008). However, M.

persicae performed as well on B. oleracea than on B. nigra and S. arvensis.

Other plant characteristics like nitrogen concentration may also have had an impact on aphid development. M. persicae has been shown to respond to phloem nitrogen levels (van Emden & Bashford, 1969; Karley et al., 2008), which are expected to be lower in cultivated than in wild species (Slansky & Feeny, 1977). Yet, in our study, the population growth rate of the aphid was not significantly different between one cultivar of B. oleracea and the two wild species B. nigra and S. arvensis. In conclusion, we cannot say which characteristics of the host plant species explained the differences in aphid development.

An alternative hypothesis to explain the differences observed in host plant suitability is a specialization of M. persicae on the Brassicaceae. The poor performance of the aphid on So.

lycopersicum might have been the result of artificial selection of clones that have specialized on Brassicaceae in the field or in the laboratory, as aphids were reared on B. oleracea for at least 10 generations. In previous studies (Vorburger, 2006; Kasprowicz et al., 2008), from aphids collected in the field, authors identified a small number of clones and at least one clone

that exhibited marked preference for Brassica crops. Thus, host plant adaptation in this aphid seems to occur, even under strong temporal and spatial variation in the availability of various vegetable and oilseed Brassica throughout the year. Moreover, this species is able to excrete (Weber et al., 1986; Merritt, 1996) or detoxify glucosinolates (Francis et al., 2005; Ramsey et al., 2010). All these studies support the fact that some clones of M. persicae might be able to specialize on Brassicaceae. Host plant specialization could explain why, in our study, aphid performance was high on wild species characterized by high concentrations of GLS, and low on non-Brassicaceae species such as So. lycopersicum. However, it does not explain why M.

persicae performed poorly on B. napus, and why it did not perform better on B. oleracea as the aphid could have adapted to this host plant.

Performance of the parasitoid D. rapae was indirectly affected by the plant on which M.

persicae was feeding but, unexpectedly, was not correlated with the performance of its host.

Gols & Harvey (2009) observed that for herbivores and parasitoids reared on different Brassicaceae, performance of the host and its parasitoid were positively correlated in most cases. We also observed a positive relationship between the performance of Brevicoryne brassicae, a Brassicaceae specialist that sequesters GLS, and D. rapae (Le Guigo et al., 2011). In this study, M. persicae adults were bigger and male parasitoids were larger on S.

arvensis (Fig. 1c and Fig. 2d), while aphids were smaller and female parasitoids were larger on B. napus. In contrast with the assumption that larger host size translates into higher quality resource for the parasitoid, and that host quality is determined by host size (Harvey, 2005), smaller hosts gave rise to larger female parasitoids. The parasitoid might have responded to differences in herbivore quality defined by other factors besides size (Harvey, 2005), or indirectly host plant species may have influenced the parasitoid's development. Moreover, whereas parasitism rate tended to be higher on both B. napus and B. oleracea, differences in development time and parasitoid size between these two species indicate that host plants might have contrasting effects on different life history traits. Further work is needed to explain the unexpected relationship between the performance of the aphid and its parasitoid, and to understand which characteristics of the host plants have an impact on the performance of the parasitoid.

Plant characteristics may have negative effects on survival and growth of some herbivore species, causing bottom-up regulation of population dynamics. Survival and reproduction of the parasitoids can also be influenced by plant characteristics through their host. Thus, plant species might also affect herbivore populations by mediating top-down regulation. Our study indicates that unexpectedly, cultivated species such as B. napus could reduce herbivore

37

performance and favour parasitoids. On the other hand, wild species such as S. arvensis could serve as reservoirs of both herbivores and parasitoids. More work on tritrophic interactions is needed to gain insights into the relative impact of cultivated and related wild Brassicaceae on the populations of herbivores and natural enemies. Whether herbivores and/or parasitoids specialize on one host plant, on a group of species or even on a landscape compartment should be investigated to determine the potential transfer of insect pests and natural enemies between cultivated and non-cultivated areas. Results may offer new perspectives for the design of systems that manage crop colonization by both herbivores and their natural enemies.

2.6. Acknowledgements

We would like to thank Michèle Travers, Ferréol Braud, and Isabelle Besse for technical assistance, Yannick Outreman for statistical advice, and Frédéric Francis for comments on a previous draft. The project benefited from suggestions by Yannick Outreman, Anne-Marie Cortesero, Emmanuel Corcket and Claire Campion. We acknowledge the French Ministry of Agriculture for funding. PLG was supported by a graduate fellowship from the region Pays-de-la-Loire (contract # 2007-7623).

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Fig 1. Development of Myzus persicae on Solanum lycopersicum (N = 29 plants), Brassica napus (N = 29), B.

oleracea (N = 29), B. nigra (N = 30), and Sinapis arvensis (N = 29). Aphids performed poorly on So.

lycopersicum and all differences between So. lycopersicum and the Brassicaceae host plant species were significant (P < 0.001). On the Brassicaceae species, significant differences in the development of M. persicae were observed for: a) the pre-reproductive period (in days), b) the adult longevity (in days), c) the adult biomass (in µg), and d) the intrinsic rate of increase (rm). Different letters indicate significant differences between host plant species.

45 Figure 1.

Fig 2. Parasitism rate and development of Diaeretiella rapae when its host Myzus persicae was feeding on Brassica napus (N = 27 plants), B. oleracea (N = 25), B. nigra (N = 28) or Sinapis arvensis (N = 28): a) Parasitism rate (%) estimated after 5 days and at mummy stage, b) Development time from egg to mummy (in days), c) Development time from mummy to adult (in days), d) Hind tibia length (µm) measured as a proxy of body size. Significant differences between host plant plant species are indicated by capital letters for the female parasitoids and lowercase letters for the males.

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B. napus B. oleracea B. nigra S. arvensis Host plant

B. napus B. oleracea B. nigra S. arvensis Host plant

B. napus B. oleracea B. nigra S. arvensis Host plant

B. napus B. oleracea B. nigra S. arvensis Host plant

Chapitre 1: Performances du phytophage spécialiste Brevicoryne brassicae et du phytophage généraliste Myzus persicae, et de leur parasitoïde commun Diaeretiella rapae sur différentes plantes hôtes

Article 2 : Impact de différentes espèces de plantes sur le développement d’un puceron